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Cephalopoda: Octopodidae): the Smallest Southwestern Atlantic Octopod, Found in Sea Debris

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Cephalopoda: Octopodidae): the Smallest Southwestern Atlantic Octopod, Found in Sea Debris A new species of pygmy Paroctopus (Cephalopoda: Octopodidae): the smallest southwestern Atlantic octopod, found in sea debris Tatiana S. Leite ( [email protected] ) Universidade Federal de Santa Catarina Centro de Ciencias Biologicas https://orcid.org/0000-0001-9117-9648 Erica A.G. Vidal Universidade Federal do Parana Setor de Ciencias da Terra Françoise Dantas Lima Universidade Federal do Rio Grande do Norte Centro de Biociencias Sergio M.Q. Lima Universidade Federal do Rio Grande do Norte Centro de Biociencias Ricardo M Dias Universidade Federal do Sul da Bahia Giulia A. Giuberti Universidade Federal do Estado do Rio de Janeiro Davi De Vasconcellos Universidade Federal do Rio Grande Jennifer A. Mather University of Lethbridge Manuel Haimovici Universidade Federal do Rio Grande Original Paper Keywords: Paroctopus, octopus Posted Date: January 29th, 2021 DOI: https://doi.org/10.21203/rs.3.rs-172910/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Version of Record: A version of this preprint was published at Marine Biodiversity on July 27th, 2021. See the published version at https://doi.org/10.1007/s12526-021-01201-z. Loading [MathJax]/jax/output/CommonHTML/fonts/TeX/fontdata.js Page 1/27 Abstract The new species, Paroctopus cthulu sp. nov. Leite, Haimovici, Lima and Lima, was recorded from very shallow coastal waters on sandy/muddy and shelter- poor bottoms with natural and human-origin debris. It is a small octopus, adults are less than 35 mm mantle length (ML) and weigh around 15 g. It has short to medium sized arms, enlarged suckers on the arms of both males and females, large posterior salivary glands (25 %ML), a relatively large beak (9 % ML) and medium to large mature eggs (3.5 to > 9 mm). The characteristics of hatchlings of two brooding females, some of their anatomical features, and in-situ observations of their behaviour are a clue to the life history of it and closely related pygmy octopuses. The Bayesian phylogenetic analysis showed that Paroctopus cthulu sp.nov. specimens grouped in a well-supported clade of Paroctopus species, separate from P.joubini and P. cf mercatoris from the Northwestern Atlantic . The description of this new species, living in a novel habitat of human debris in shallow water off Brazil, offered an opportunity not only to evaluate the relationship among the small octopuses of the western Atlantic, Caribbean and eastern Pacic, but also their adaptation to the Anthropocene period. Introduction The pygmy octopuses are smallbodies species of Octopodidae, some of which mature as small as 20 mm dorsal mantle length (around 100 mm total length). Most of them are currently placed in the genus Paroctopus. This genus was originally proposed by Naef (1923) based on the relatively large size of the eggs of Paroctopus digueti Perrier & Rochebrune, 1894 (capsule length 10 mm) . Two years later, Grimpe (1925) erected the genus Pseudoctopus based on the same morphotype species, citing the single attachment of eggs, as well as the egg size. Naef discarded the genus name Paroctopus in 1928, apparently because he felt it was not valid, although he did not discuss the reasons for such a decision. Robson (1929) resurrected the name, but had reservations about erecting a new genus based solely on egg size. In an attempt to validate Naef’s genus, he amplied the diagnosis with several additional characters, namely: 1) possession of relatively long copulatory organ (Ligula length index LLI 720); 2) short arms and 3) squat, bursiform body. Pickford (1945, 1946) initially accepted the validity of the genus in her evaluation of the octopodine fauna of the western Atlantic. However, she later rejected the name when discussing the generic placement of the large-egg species, Octopus bimaculoides Pickford & McConnaughey, 1949. As currently understood, the genus is represented by a transisthmian geminate species complex endemic to tropical and subtropical waters in the Americas (see Berry 1953, Nesis, 1975, 1978, Lima et al.2020). This complex includes Paroctopus digueti (type species) along the tropical eastern Pacic, and two morphotypes: one with smaller eggs (< 4 mm) and the other with larger eggs (>5 mm) in the Northeastern Atlantic, Caribbean Sea and Gulf of Mexico (Forsythe and Hanlon, 1980; Tiffany et al.2006). Due to their small size, the pygmy octopuses have been used in laboratory experiments on mating behavior (Mather 1978; Cigliano 1995); reproductive biology and growth (Opresko and Thomas, 1975) and ontogeny of behavior, habitat use and distribution (Mather 1980a, 1980b, 1982a, 1982b, 1984). When it comes to the Northwestern Atlantic and Caribbean Sea, the pygmy taxonomy is mixed up. In the Caribbean Sea (St. Thomas/ Virgin Island), the smallegged species was described as Octopus joubini Robson 1929 (Robson 1929) and a broad literature citing this species is available (Pickford 1945, Boletzky and Boletzky 1969. Forsythe 1984). However, some important publications cited the largeegged species also under the name O. joubini (Opresko and Thomas 1975, Hanlon 1983). Other studies refer to a pygmy octopus with large eggs from the Gulf of Mexico (Dry Tortugas and Tampa Bay) as Octopus mercatoris Adam, 1937 (Forsythe and Hanlon 1980, Forsythe and Toll 1991, Tiffany et al. 2006), despite the fact that the holotype of O. mercatoris is a female bearing relatively small eggs (3 mm) (Voss and Toll 1998). In fact, some authors considered the smallegged species, O. joubini and O. mercatoris, as possible Paroctopus (Voss and Toll1998, Jereb et al.2014, Lima et al.2020), while the largeegged species is still undescribed. The available literature on pygmy octopuses from the Southwestern Atlantic is scarce and not less confusing. Haimovici (1985) registered as O. joubini a small juvenile collected in a tide pool off Vitória, Espirito Santo State. Perez and Haimovici (1991) designated as O. joubini a lot of small octopods (MZUSP 27028) collected in São Paulo State (23o 30´S) in their list of cephalopod species deposited at the Zoology Museum of the University of São Paulo. In recent years, several small adult octopuses with stocky bodies and medium sized arms, some of them bearing the enlarged suckers and a medium size ligula, that ts the description of the Paroctopus type species, were collected in shallow waters of Santa Catarina and Rio de Janeiro states, along the temperate Brazilian coast. Live specimens were observed using human garbage as shelters. They included two brooding females with medium to relatively large eggs, which enabled the descriptions of eggs, embryos and hatchlings and thus provided biological and ecological information on the early stages of the life cycle. Morphological features and body proportions of eggs and hatchlings in relation to those of the adults are important for inferences about the developmental mode – planktonic or benthic – of octopus hatchlings, providing key information on life history traits. Genetic and morphological characterization of these specimens does not t with the available information on the described species of the genus and support their description as a new species. Additional images and videos provided valuable information on their behavior. Herein, we provide a detailed and integrated description of a new species of Paroctopus collected from sea garbage, including descriptions of adult males and females, eggs, embryos and hatchlings, along with molecular data and analyses. Materials And Methods Collection samples A total of 12 specimens (six adult males; three adult females and three juveniles) was collected in the shallow coastal waters of Rio de Janeiro municipality and Ilha Grande continental island (Angra dos Reis municipality) in Rio de Janeiro (RJ) State, and in Porto Belo municipality in Santa Catarina (SC) State, Central and Southern Brazil (Fig. 1a and b). Most of the RJ specimens were collected at depths shallower than 5 m by hand, during snorkeling or SCUBA diving on rubble or sandy bottoms near the rocky coast. The temperature varied from 19 to 26 o C. The specimens were collected by sorting solid garbage Loading [MathJax]/jax/output/CommonHTML/fonts/TeX/fontdata.js Page 2/27 found on the sea bottom, including metallic cans, glass bottles and plastic objects such as snorkeling mouthpieces, among others. No specimen was found inside empty shells, although we looked for them, also 9 divers. Two females with eggs were found, one spawned inside a snorkeling mouthpiece and the other in a metal beer can. Morphological data Most specimens were xed in 10% formalin and preserved in 70% ethanol. Measurements, counts and indices followed Roper and Voss (1983) and Huffard and Hochberg (2005). Sucker counts included all suckers in each arm, rather than only those on the basal half. The following abbreviations are used for measurements and indices: AFL: left arm formula, AFR: right arm formula, ALI: arm length index (arm length/ML × 100), ASC: arm sucker count (number of suckers of each designated arm), AWI: arm width index (arm width at the widest point on stoutest arm/ML × 100), CaLI: calamus length index (calamus length/LL ×100), FLI: funnel length index (funnel length/ML × 100), FFLI: Free funnel length index (free funnel length/funnel length x 100); GiLC: gill lamellae count per demibranch, HLI: hectocotylus length index (hectocotylus length/hectocotylized arm length x100; HWI: head width index (head width/ML × 100), LLI: ligula length index (ligula length/HL × 100), ML: dorsal mantle length,
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